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The Functions and Importance of CH···O Bonds in SET Domain Methyltransferases

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The Functions and Importance of CH···O Bonds in SET Domain Methyltransferases The Functions and Importance of CH···O Bonds in SET Domain Methyltransferases by Scott A. Horowitz A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Biophysics) in The University of Michigan 2013 Doctoral Committee: Professor Hashim M. Al-Hashimi, Co-Chair Associate Professor Raymond C. Trievel, Co-Chair Professor Charles L. Brooks III Assistant Professor Tomek Cierpicki Professor Anna K. Mapp © Scott Horowitz 2013 Acknowledgements I would like to first and foremost thank Profs. Ray Trievel and Hashim Al- Hashimi. I consider myself lucky to have been able to learn two different approaches to a scientific problem from two tremendous scientists. I would also like to thank my dissertation committee for their many useful suggestions over the years. I would like to thank everyone from the Trievel and Al-Hashimi groups, many of whom have aided and taught me over the years. In particular, Paul Del Rizzo taught me much of what I know about working with proteins and biochemistry, and Jennifer Nimtz was extremely helpful in protein crystallization. Alex Hansen has given me enormous support learning advanced NMR concepts, and most importantly, Joseph Yesselman has been an enthusiastic collaborator on many facets of this work, without whom I would not have been able to complete much of what is presented here. Also, many collaborators from outside the university have been instrumental in this work. Most notably, Lynnette Dirk and Bob Houtz performed the radiometric assays, and gladly took up each new challenge as it came. Also, the advice of Ryan Mehl provided essential advice on making protein with unnatural amino acids and the help of Sam Butcher and Kirk van der Meulen helped us considerably with ITC analysis. And last but not least, Doug Markham was responsible for helping all of this get started in the first place with his gift of the AdoMet synthetase enzyme. ii Table of Contents Acknowledgements ..................................................................................................................... ii List of Tables ................................................................................................................................ iv List of Figures ............................................................................................................................... v List of Appendices .................................................................................................................... viii Abstract......................................................................................................................................... ix Chapter 1 : Introduction .............................................................................................................. 1 Chapter 2 : Direct Evidence for Methyl Group Coordination by CH···O Hydrogen Bonds in SET Domain Methyltransferases ......................................................................................... 27 Chapter 3 : CH···O Hydrogen Bonds Mediate AdoMet-Dependent Methylation............ 43 Chapter 4 : Conclusions and Future Directions ..................................................................... 79 Appendix A ................................................................................................................................. 87 References ................................................................................................................................... 98 iii List of Tables Table 2.1 Dissociation constants and binding enthalpies of AdoMet, Sinefungin, and AdoHcy to SET7/9 ...................................................................................................................... 40 Table 3.1: Crystallographic statistics for structures of SET7/9 Y335pAF•TAF10•AdoHcy, SET7/9 Y335F•TAF10•AdoHcy, SET7/9•TAF10 K189A•AdoHcy, and SET7/9•TAF10 K189A•AdoMet. ...................................................... 63 Table 3.2: WT SET7/9 and mutants Y335pAF, Y335F dissociation constants and catalytic parameters. .................................................................................................................................. 68 Table 3.3: All AdoMet-C8···Tyr335-OH distances in high-resolution (<2.0 Å) SET7/9 crystal structures. ....................................................................................................................... 70 iv List of Figures Figure 1.1 AdoMet chemical structure ...................................................................................... 2 Figure 1.2: SN2 mechanism of AdoMet-dependent methyl transfer.................................... 3 Figure 1.3: Example of “loose” and “tight” transition states. ................................................ 4 Figure 1.4: SET domain architecture. ........................................................................................ 8 Figure 1.5: Oxygen-lined pore of SET domain methyltransferase. ....................................... 9 Figure 1.6: Distance and angular parameters used when defining CH···O hydrogen bonds. ........................................................................................................................................... 11 Figure 1.7: Timeline of important events in the history of CH···O hydrogen bonding research. ....................................................................................................................................... 13 Figure 1.8 Examples of CH···O hydrogen bonds (orange dashes) in proteins. ................. 15 Figure 1.9: Examples of CH···O hydrogen bonds (orange dashes) in nucleic acids. ........ 17 Figure 1.10: Examples of CH···O hydrogen bonds (orange dashes) in molecular recognition and enzyme catalysis. ........................................................................................... 18 Figure 1.11: Crystal structure of SET7/9 bound to AdoMet (47, 49). .................................. 26 Figure 2.1: 2D-HSQC of SET7/913C-methyl AdoMet complex ........................................... 34 Figure 2.2: Free AdoMet in implicit solvent. .......................................................................... 35 Figure 2.3: Optimized and broken CH···O hydrogen bonds in SET7/9.............................. 36 Figure 2.4: Chemical shift of the AdoMet methyl group as a function of rotation angle.37 v Figure 2.5: Binding modes of AdoMet (A), Sinefungin (B), and AdoHcy (C) to SET7/9 are nearly identical. .................................................................................................................... 39 Figure 2.6: ITC analysis of AdoMet binding to SET7/9. ....................................................... 40 Figure 3.1: Selective 13C R1ρ relaxation and relaxation-dispersion pulse sequence for 13CHD2-methyl groups. ............................................................................................................. 53 Figure 3.2: 13C R1 relaxation pulse sequence for 13CHD2-methyl groups. .......................... 53 Figure 3.3: Methyl CH···O hydrogen bonding in AdoMet-dependent methyltransferases. ....................................................................................................................................................... 57 Figure 3.4: Angular distribution of methyl CH···O hydrogen bonds. ................................ 59 Figure 3.5: Distance and angular distribution of methylene CH···O hydrogen bonds. ... 59 Figure 3.6: Calorimetric analysis of SET7/9 Y335pAF. ............................................................. 61 Figure 3.7: Structure of the SET7/9 Y335 mutants bound to AdoHcy and the TAF10 peptide. ........................................................................................................................................ 62 Figure 3.8 Ligand binding modes of WT and SET7/9 Y335pAF are conserved. ............... 63 Figure 3.9: Model of SET7/9 Y335pAF hydrogen positions based on its crystal structure and density functional theory calculations. ........................................................................... 65 Figure 3.10: WT SET7/9•AdoMet and SET7/9 Y335F•AdoMet methyl 1H chemical shift measurement. ............................................................................................................................. 66 Figure 3.11: Representative injection peak and best-fit kinetic parameter trace from AdoMet•WT SET7/9 ITC experiments. .................................................................................. 66 Figure 3.12: Measurement of cofactor binding affinity by intrinsic tryptophan fluorescence................................................................................................................................. 68 Figure 3.13: Radiometric methyltransferase assays with varying AdoMet concentration. ....................................................................................................................................................... 69 Figure 3.14: Triplicate single turnover experiments on SET7/9 at 37° C. ........................... 69 Figure 3.15: Quantum chemistry geometry optimizations and interaction energies of AdoMet and methyl transfer transition state CH···O hydrogen bonds. ............................ 73 vi Figure 3.16: Methyl transfer pore contraction in SET7/9. ........................................................... 75 Figure 3.17: (A) R2 and (B) R1 13C spin relaxation fits of 13CHD2-methyl AdoMet bound to SET7/9. ....................................................................................................................................
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